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1
Review
.
Article
.
Oriental Cholangiohepatitis: Radiologic Features
Pathologic,
Clinical,
and
Jae Hoon Lim1
Oriental cholangiohepatitis, an endemic disease in Southeast Asia, is characterized by recurrent attacks of abdominal pain, fever, and jaundice. Pathologically, the intra- and extrahepatic ducts are dilated and contain soft, pigmented stone and pus. There is proliferation of bile ducts and infiltration of inflammatory cells along the periportal spaces and hepatic parenchyma. Localized intrahepatic segmental ductal stenosis may be present, especially in the lateral segment of the left lobe or posterior segment of the right hepatic lobe. The cause of the disease is not known, but associations with clonorchiasis, ascariasis, and nutritional deficiency have been suggested. Sonographic and CT findings include intra- or extrahepatic duct stones, dilatation of the extrahepatic duct with relatively mild or no dilatation of the intrahepatic ducts, localized dilatation of the lobar or segmental bile ducts, increased periportal echogenicity, segmental hepatic atrophy, and gallstones. Cholangiographic findings include bile duct stones; disproportionately severe dilatation of the extrahepatic ducts with mild or no dilatation of the intrahepatic ducts; and focal strictures, acute peripheral tapering, straightening, ngidity, decreased arborization, and an increased branching angle of the intrahepatic bile ducts.
Oriental cholangiohepatitis (OCH), also known as oriental cholangitis, recurrent pyogenic cholangitis, and intrahepatic pigmented stone disease, is characterized by recurrent attacks of fever, chills, abdominal pain, and jaundice [1-4]. Bile ducts are dilated or focally stenotic, harboring soft, pigmented stone or mud, and enteric bacteria can be cultured from the bile [1-3, 5]. The wall of the bile ducts is thickened by fibrosis and inflammatory cell infiltration. The disease is endemic to Received
December
Department
26, 1990;
of Diagnostic
accepted
Radiology,
after Kyung
revision
February
Hee University
Southeast
Asian countries [1-5], but sporadic cases have in Europe [6] and South Africa [7]. The disease encountered more often in western societies, especially in the United States and Canada, largely as a result of increased immigration from Asian countries [4, 5]. The purpose of this article is to review the sonographic, CT, and cholangiographic findings of OCH in light of the pathophysibeen reported is now being
Fig. 1.-Microphotograph of resected liver specimen shows soft, pigmented stone (long arrow) in dilated medium-sized bile duct. Note also severe thickening of small bile ducts and periductal fibrosis (short arrows) obliterating lumen of bile ducts and encroaching on hepatic parenchyma. (Masson’s trichrome stain, original magnification x8)
14, 1991.
Hospital,
1, Hoeki-dong,
LJm. AJR 157:1-8,
July
1991 0361-803X/91/1571-0001
© American
Roentgen
Ray Society
Dongdaemun-ku,
Seoul
130-702,
Korea.
Address
reprint
requests
to J. H.
LIM
2
ology of the disease and to discuss the management of the disease.
the radiologist’s
role in
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Pathology
The primary pathologic changes are in the bile ducts. Histologically [1 2, 8], there is proliferation of bile ducts, and inflammatory cells, mostly polymorphonuclear leukocytes, infiltrate from the portal tracts well into the hepatic parenchyma, accompanied by local hepatocellular necrosis. In more severe cases this inflammation undergoes suppuration. Fibrous tissue proliferates in the portal tracts, especially around the bile ducts (Figs. I and 2). The intrahepatic ducts frequently show dilatation and stricture and may contain pigmented stone (Fig. 1), pigmented mud, and debris and may shed epithelial cells, exudates, and sometimes frank pus. Liver changes are common and can be quite severe [2, 9]. The liver is usually enlarged and scarred, and capsular adhesions are evident. Occasionally, after multiple attacks, the liver becomes shrunken, especially the lateral segment of the left lobe. The papilla is usually hypertrophied [2], fibrosed, and rigid but ,
patent,
allowing
passage
of a large
dilator
without
difficulty
[9]. In some cases there is penampullary stricture due to fibrosis and passage of stone. Dilatation of the extrahepatic ducts and large intrahepatic ducts such as the right and left hepatic ducts is observed in most patients (85-1 00%) [1 0, 1 1]. Dilatation of the intrahepatic biliary ducts tends to be disproportional, that is, central dilatation with rapid tapering toward the periphery [1 0]. The first and second divisions of the ducts are dilated, whereas the third and fourth divisions are not. The cause is not known, but periductal diffuse fibrosis may play a role (Fig. 2). This pattern
of bile duct
dilatation
is quite
different
from
the dila-
tation caused by obstruction. In obstruction, the intrahepatic bile ducts are dilated diffusely instead of rapidly tapering peripherally. The dilatation of the extrahepatic duct generally is not related to the location of the stone [1 1]. Ducts both proximal and distal to the stone are dilated diffusely. Repeated passage of small pieces of stones through the sphincter of Oddi into the duodenum results in hypertrophy, ulceration, and stricture [2],
and these
changes
may
cause
stenosis
and
MR:157,
July 1991
hepatic ducts or both. Occasionally the bile ducts are packed with stones. Bile duct stones are present in about 75-80% of cases [2, 9]. In the remaining cases, the biliary tree is infected recurrently in the absence of stone. Gallstones are found frequently, and including the cases of previous cholecystectomy, gallstones are present in about 50-70% [10-12]. The reported prevalence of cholangiocarcinoma associated with
OCH
ranges
from
2.4%
to
5.0%
[1 4,
15].
Chronic
proliferative cholangitis in the presence of bile duct can undergo progressive changes to atypical epithelial plasia,
which
may
progress
to cholangiocarcinoma
stones hyper[1 6]. To
my knowledge there has been no report on an increased prevalence of hepatocellular carcinoma in patients with OCH.
Pathogenesis
Two theories esis of OCH.
have been advanced Chronic
infestation
to explain the pathogen-
of the biliary
tree
with
en-
demic parasites such as Clonorchis sinensis and Ascaris lumbricoides may induce ductal injury and strictures, leading to stone formation. Many patients with intrahepatic stone have evidence
tation
of clonorchiasis
with Ascaris
Microscopic
sections
[1
is observed of stones
,
1 7, 1 8]. Evidence
in patients from
extra-
with
of infes-
OCH
[7].
and intrahepatic
bile ducts revealed evidence of C. sinensis (Fig. 3) and A. lumbricoides [1 1 9]. As adult flukes or Ascaris eggs and ,
desquamated
epithelial
cells block
the intrahepatic
ducts
par-
tially or completely, tion favors bacterial
bile stasis is sure to follow [17]. Stagnainfection resulting in pyogenic cholangitis. pyogenic infection occurs in the bile ducts, C. sinensis are killed [17, 20]. Bile stasis and the presence of dead and ova or their debris can form a nucleus (Fig. 3) for
When flukes flukes the formation of gallstones or bile duct stones [19], and this could instigate all the consequent pathologic processes, resuiting in a cycle of repeated bouts of cholangitis and stone formation [3]. The formation of bilirubin stones may be attributed to bacterial deconjugation of bilirubin diglucuronoside
proximal
dilatation. However, localized stricture and resultant dilatation of the intrahepatic ducts are closely related to the location of stones. The left lateral segmental duct is affected earlier and more severely [2, 1 1 1 2], followed by the posterior segmental duct of the right lobe [12]. This may be related to the more acute angulation of these ducts, resulting in less efficient drainage on this side of the biliary system [2, 12]. Stricture along the extrahepatic ducts is very unusual [2]. The bile duct stones encountered in western persons originate in the gallbladder and have the same chemical composition as gallstones [13]. On the other hand, the stones in ,
patients with OCH originate in the bile ducts and are composed mostly of bile pigment with variable calcification. The stones are dark brown or black and vary in consistency from claylike, muddy material to concrete stones that are usually soft and friable [2, 3, 9]. There may be single or multiple stones. Multiple stones are scattered in the intra- or extra-
Fig. 2.-Cut surface of resected lateral segment of left hepatic lobe shows marked fibrous thickening of segmental bile duct (open arrows) and its tributaries. Hepatic veins (solId arrows).
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MR:157,
ORIENTAL
July 1991
CHOLANGIOHEPATITIS
with the formation of insoluble bilirubin during bouts of cholangitis [21]. Ong [2], however, found that patients with OCH had only a 5% higher rate of infestation with C. sinensis than did patients in general outpatient clinics. Large proportions of persons in endemic areas are infested with liver flukes without pyogenic cholangitis developing [8]. It was proposed that the primary cause was portal septicemia resulting from poor eating habits [2, 4]. Ong [2] believed infection reached the biliary tract from the portal vein: “The infection having reached the liver is excreted into the bile. Should there be obstruction by C. sinensis, tumor or stones, cholangitis would be the result.” This theory was supported by animal experiments [8]. Bilirubinate stones may be formed in the liver as a result of an increase in deconjugation of bilirubin glucuronide by Escherichia co/i, attributed to a net increase in f.-glucuronidase activity. This arises when the intrahepatic environment is deficient in glucaric acid, a fl-glucuronidase inhibitor that is lacking in a low-protein diet [22]. These two theories cannot explain the pathogenesis of OCH. Perhaps both factors play a role separately or synergistically.
Clinical
Manifestations
Men and women are affected almost equally [2, 9] and the highest number of cases occur in persons 20-40 years of age. There is a strong association with lower socioeconomic class. The symptoms are recurrent attacks and remissions of abdominal pain, nausea, vomiting often accompanied by fever, shaking chills, and jaundice. Visible jaundice is present in 77% of patients [2]. Physical examination reveals epigastric tenderness and rigidity and enlargement of the liver and gallbladder. Occasionally patients with severe disease such as sepsis present with shock and mental confusion. Laboratory findings are leukocytosis, predominantly polymorphonuclear leukocytes; elevated levels of alkaline phosphatase; and excretion of urobilinogen in urine. Bile cultures yield E. co/i or other enteric bacteria. The natural history of the disease is marked by recurrent attacks of cholangitis, usually once or twice a year [2, 9]. Many of the acute attacks respond to antibiotic treatment; many also require decompression of the biliary tree after control of the acute attack [2, 9], especially when there is a stone or stricture of bile ducts. OCH is a frequent reason for emergent surgery in the endemic areas. Recurrent disease is common postoperatively, especially when the operation does not include a drainage procedure [4, 23-25]. Even after surgery with drainage, stones and stricture return and the attacks of cholangitis recur sooner or later. In a study of 115 patients who had had surgery, 66 patients (57%) had residual intrahepatic stones [26]; biliary stricture caused the remnant stone in the majority of cases (81%).
Radiologic
Fig. 3.-Microphotograph embedded In pigmented
stone.
shows eggs of Clonorchls slnensls (arrows) (H and E, original magnification xlOO)
Fig. 4.-Sagittal sonogram shows dilatation of common bile duct containing three shadowing stones (arrows). Wall of common bile duct (D) is thick.
Fig. 5.-Transverse sonogram of liver shows a shadowing echogenic cast filling posterior segmental bile duct of right hepatic lobe (arrows).
3
Findings
Radiologic assessment of the biliary tree is imperative if the correct preoperative evaluation is to be made regarding the need for and the type of surgery [4, 25]. Plain radiography is not helpful because the stones are rarely radiopaque [2, 6, 7, 12]. Oral cholecystography, IV cholangiography, and biliary scintigraphy are not useful [2,27]: correct anatomic diagnosis cannot be made even if the biliary tract is visualized.
4
LIM
MR:157,
July 1991
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Fig. 6.-Transverse sonogram of common bile duct shows a round, nonshadowing stone (arrow). Proximal and distal portions of bile duct are dilated diffusely (arrowheads). A = abdominal aorta, v = inferior vena cava.
Fig. 7.-Transverse sonogram of left hepatic lobe shows thickening and increased echogenicity of walls of bile ducts (arrows) and umbilical portion of left portal vein (P).
Sonographic
Findings
Sonography delineates bile duct dilatation in virtually all patients with OCH. The extrahepatic bile ducts are dilated in 85-100% of cases and the larger intrahepatic bile ducts are dilated in 66-79% of cases [1 0, 1 1 ]. Usually, the smaller intrahepatic bile ducts such as the tertiary or quaternary divisions proximal to the segmental bile ducts are dilated only slightly or not at all. In general, the dilatation of the extrahepatic duct is not related to the location of stone [1 1], although localized dilatation of the intrahepatic ducts is closely related to the location of stricture and stone Iodgment, especially the lateral segmental ducts of the left hepatic lobe [1 1]. In a large proportion of patients with OCH (85-90%), a stone or stones can be detected with sonography [1 0, 1 1]. The stones may be in either the extrahepatic (Fig. 4) or intrahepatic (Fig. 5) ducts or both. In some cases, stones are only in the segmental bile ducts, such as the lateral segment of the left hepatic lobe or posterior segment of the right hepatic lobe (Fig. 5). The stones may be more echogenic than the liver parenchyma Some
and
adjacent
usually
echogenic
tissue
or,
less
commonly,
isoechoic.
stones cast shadow and some do not, even in the same patient [1 0, 1 1]. In general, the intrahepatic stones are extrahepatic
and
shadowing
(Fig.
5), whereas
some
stones
(25%) do not cast shadow (Fig. 6). This may be due to the poor rate of detection of the intrahepatic stones, because hypoechoic intrahepatic stones without shadows can be missed on sonography. The detectability of stones with sonography depends on the size, echogenicity, shadowing characteristics, and location of the stones [11, 28]. Biliary mud or isoechoic bile duct stones filling the biliary tree as a cast can be missed because sometimes they appear as soft-tissue masses and obscure visualization of intrahepatic ductal dilatation [10, 25, 29]. Biliary pneumatosis, as a result of prior choledochoenteric anastomoses or sphincter incompetency, obscures visuali-
zation of stone. A higher proportion of nonshadowing stones in the extrahepatic ducts can be detected compared with intrahepatic stones [10, 11]; this is because the duct is dilated, providing a larger space to enable the nonshadowing stone to be detected (Fig. 6).
Fig. around
8.-CT ports
scan hepatis,
shows dilatation of central intrahepatic with bile ducts tapering abruptly toward
bile ducts periphery.
Chau et al. [1 0] described prominent periportal echogenicity (Fig. 7) representing pericholangitis and periportal fibrous thickening in 30% of their cases. Gallstones are found frequently patients
[1 0, 1 1]. Hepatic abscess or biloma complications with OCH can be delineated on sonograms.
in
CT Findings The optimal CT technique
is enhanced
scanning
with a slice
thickness scanning
of 5 mm and 2-mm interslice gap. Unenhanced may be helpful in detecting stones. CT demonstrates the full extent of ductal dilatation [12]. Dilatation of the extra-
hepatic ducts is depicted clearly. Central, larger intrahepatic biliary dilatation; acute peripheral tapering; and nonvisualization toward the periphery of the liver give rise to the characteristic arrowhead appearance on contiguous sections (Fig. 8). There may be localized dilatation from obstruction by stricture (Fig. 9) or stone, such as that of lateral segmental ducts of the left hepatic lobe and posterior segmental ducts of the right hepatic lobe [12]. However, biliary strictures,
which are usually
short
segments,
are difficult
to depict
be-
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MR:157,
July 1991
ORIENTAL
5
CHOLANGIOHEPATITIS
Fig. 9.-Multiple intrahepatic stones in lateral segment of left lobe and extrahepatic stone. A, Transverse sonogram of epigastrium shows shadowing echogenic foci (short arrow). Note moderate dilatation of subsegmental bile duct with thick wall (long arrow). B, CT scan of liver shows localized severe dilatation of lateral segmental bile duct of left hepatic lobe due to localized stricture (arrow). Multiple tiny high-density areas within dilated duct represent small stones that might have been overlooked on basis of CT alone. Wall of dilated bile ducts is enhanced. C, CT scan at level of pancreatic head shows small, round, calcified stone (arrow) within dilated intrapancreatic common bile duct.
Fig. 10.-CT scan shows cystically dilated bile duct containing stone. Wall of dilated bile duct is enhanced. Biliary pneumatosis (arrow). The patient had had a cholecystectomy.
Fig. 11.-Enhanced CT scan shows homogeneous enhancement of left lobe of liver. Walls of bile ducts are enhanced (long arrows). lntrahepatic stones (short arrows) have same attenuation as liver. PV = right branch of portal vein.
Fig. 12.-CT scan shows severe atrophy of lateral segment of left hepatic lobe harboring small calcific stones (open arrow).
cause of partial-volume averaging. Sometimes, dilatation may be fusiform or cystic (Fig. 10). The wall of the bile ducts may enhance on CT scans obtained with contrast material (Figs. 9 and 10), especially during an acute cholangitic episode [12]. The stones can be depicted with CT, but the detection rate (63-81%) is generally not as good as that of sonography [6, 30]. It has been stated that unlike cholesterol stones, which may be isodense with bile, pigmented stones are hyperdense on CT (Fig. 9C) because of their variable content of calcium salts, heavy metals, and other inorganic components [29, 30].
completely fill the ducts within the hepatic parenchyma (Fig. 11) could easily be missed on CT; in these patients, even the dilated bile ducts are difficult to recognize. Chan et al. [12]
However, bile duct stones are sometimes not sufficiently hyperdense to be visualized on CT (Fig. 11). Often the stones are hypodense, and thus it is impossible to distinguish stones
exacerbation,
from bile or pus in the dilated duct [30]. Isodense
stones that
described both unenhanced and enhanced scans as desirable because stones are detected more easily on unenhanced scans, and enhanced CT scans are better in the detection of
subtle intrahepatic biliary dilatation. In addition to the ductal change and detection of stones, parenchymal loss and segmental atrophy (Fig. 12) can be correctly assessed with CT [12]. During the stage of acute persistent
segmental
or lobar
parenchymal
en-
hancement can be observed (Fig. 11), suggesting diffuse parenchymal inflammation or microabscess [12]. Frank hepatic abscess or biloma can be delineated.
LIM
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6
AJR:157,
July 1991
Fig. 13.-Endoscopic retrograde cholanglogram shows three stones with facets. Extrahepatic ducts are markedly dilated. Right and left hepatic ducts and their first divisions are moderately dilated but more peripheral ducts taper abruptly. Intrahepatic bile ducts show straightening and rigidity, right angle branching pattern, decrease in arborization, and acute peripheral tapering. (Reprinted from Lim et al. [11].)
Fig. 14.-Endoscopic retrograde cholanglogram shows mild dilatation of extra- and intrahepatic bile ducts with abrupt peripheral tapering, straightening, and increased angle of branching. Three small faceted stones are seen in common bile duct (whIte arrows). Lateral segmental bile duct of left hepatic lobe is diffusely dilated and harbors multiple filling defects of stones (arrowheads). Note mild stricture at juncton (black arrow) of lateral segmental duct and left lobar ducts.
ducts (Figs. 13 and 1 4). When the stones completely obstruct the orifice of the segmental or subsegmental bile ducts (missing duct sign), the stone cannot be detected (Fig. 15). Similarly, when there is a stricture at the segmental or subsegmental bile ducts, proximal bile ducts cannot be opacified, leading to an erroneous interpretation of no ductal stone or stricture [27]. A few patients (15-25%) have no stones, or stones pass spontaneously [2]; in these patients, the characteristic pattern of the biliary tree will lead to the correct diagnosis [35].
diagnosis between gallstones passed into the extrahepatic duct and OCH is very difficult. The stone passed only into the extrahepatic duct from the gallbladder usually will result in dilatation mainly proximal to the stone [34], whereas in OCH the extrahepatic ducts both proximal and distal to the stone are dilated diffusely regardless of the level of the stone [33, 35]. Clonorchiasis, another prevalent infestational disease in the same endemic areas, causes diffuse dilatation of the intrahepatic bile ducts with no or minimal dilatation of the large bile ducts; these changes are easily recognizable on sonography [1 8], CT [36], and cholangiography [37, 38]. Periductal changes are encountered in both diseases, but are much more severe in clonorchiasis. Stones and flukes of C. sinensis can be differentiated easily. In biliary obstruction by malignant tumors along the bile ducts, including cholangiocarcinoma and cancer of the pancreas or ampulla of Vater, the entire biliary tree proximal to the mass is dilated, including peripheral intrahepatic bile ducts, and an obstructing mass can be detected [1 1 8, 38]. Sclerosing cholangitis may show bile duct dilatation and thickening of all of the bile ducts, but dilatation is focal and discontinuous, sometimes having a beaded appearance and serpiginous course [39]. Caroli disease is a developmental anomaly in which there is segmental saccular dilatation of the intrahepatic ducts. This results in stasis, cholangitis, liver abscess, and stone formation. The clinical picture is similar to that of OCH, but it occurs in a younger age group. Differentiation is possible by noting the dilated saccules in the intrahepatic bile ducts [40, 41].
Differential
Relative Roles of Imaging
Cholangiographic
Findings
Direct cholangiography, such as endoscopic retrograde cholangiography, percutaneous transhepatic cholangiography, operative cholangiography, and T-tube cholangiography, demonstrates the full spectrum of ductal changes and stones in patients with OCH (Fig. 13). Abnormal findings include disproportionately severe dilatation of the extrahepatic ducts with mild or no dilatation of the intrahepatic ducts and acute tapering, straightening, rigidity, increased or right-angle branching pattern, multiple focal strictures, and decrease in arborization [31 -35]. These abnormalities are due to fibrosis and scarring of bile ducts [5]. Biliary duct dilatation is segmental or subsegmental [31 ] when there is stricture of intrahepatic bile ducts or obstruction by impacted stone (Fig. 14). Stricture of the extrahepatic bile ducts may occur, but this is unusual. Rarely, the segmental or subsegmental bile ducts dilate cystically because of persistent obstruction, resultant inflammation, and loss of the elasticity of the ducts. Stones
produce
negative
filling defects
in the opacified
bile
,
Diagnosis
From the radiologic point of view, OCH is characterized by the presence of stone(s), dilatation of the extrahepatic ducts, large intrahepatic bile ducts with acute peripheral tapering, and thickening of the wall of bile ducts. Knowing these features, radiologic differentiation from other diseases of the bile ducts can be possible. In western patients, the differential
Tests
Sonographic evaluation of extrahepatic bile duct dilatation is easy, although duodenal gas sometimes hinders the visualization of the whole segment, especially the distal common bile duct. Most intra- and extrahepatic stones are recognized easily. However, those stones that do not cast an acoustic shadow are difficult to recognize unless corresponding ducts
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AJR:157,
ORIENTAL
July 1991
7
CHOLANGIOHEPATITIS
Fig. 15.-Remnant stone after surgical removal of some stones. A, Sonogram of right hepatic lobe discloses a bandlike shadowing stone (arrows) filling posterior segmental bile duct. B, During surgery, several small pigmented stones were removed. Operative cholangiogram does not show any stone in biliary review suggests an area is devoid of bile ducts (missing duct sign, arrow) in lateral part of right hepatic lobe. C, T-tube cholangiogram discloses large stones packing markedly dilated posterior segmental duct of right hepatic lobe (arrows). posterior segmental duct joining right hepatic duct.
Retrospective
Note
hairpin
turn of
are markedly dilated [1 0, 1 1 ]. Bile duct stricture cannot be demonstrated easily. In the presence of biliary pneumatosis, bile ducts and stones are difficult to assess [25, 29]. CT demonstrates the full extent of ductal abnormality [12]. Biliary dilatation and isolated segmental or subsegmental
Role of Interventional
biliary
usually is essential [23-25]. In emergent cases with increased risk of surgical mortality, biliary decompression with a percu-
dilatation
can
be recognized
easily.
However,
it is
relatively insensitive in depicting stones. Pneumatosis, parenchymal enhancement, and segmental atrophy can be assessed by CT. However, biliary strictures, which usually are less than 1 cm long or are diaphragmlike, and ductal wall irregularities often are not diagnosed with CT [12]. Cholangiography
the biliary sometimes especially
is straightforward,
as it directly
delineates
tree, including stones and strictures. However, it is difficult to visualize the whole biliary tree, when
there
is technical
failure
in the opacification
of the whole biliary tree or obstruction due to ductal stricture or impaction of stones, leading to an erroneous normal interpretation. Sonography should be the main technique used for screening and diagnosis in suspected OCH [10-12, 27, 29]. CT is not a screening procedure, but it is recommended when sectional imaging is mandatory but sonography is not confirmative or is equivocal, when space-occupying lesions complicate OCH, when hepatic resection is planned, and when imaging guidance is needed for complex drainage procedures or formation of safe access to an anastomotic loop of a bowel [12]. Direct cholangiography, although invasive, is mandatory as a “road map” in patients undergoing surgical intervention, because the exact location and number of stones and bile duct strictures must be assessed preoperatively [6]. Cholangiography is necessary for the detection of residual stones after surgery, assessment of biliary stricture and choledochoenteric fistulas, and preprocedural biliary intervention [25, 26].
Radiology
tree.
in the Management
of
Bile Duct Stones Surgery controlled
taneous
used to remove stones after [2, 9]. At surgery, an internal
catheter
is the procedure
acute cholangitis is drainage procedure
of choice.
There are several nonsurgical means of treating bile duct stones and stricture. Flexible choledochoscopy and endoscopic papillotomy [42] have been used to remove postoperative residual stones. Recently, percutaneous removal of stones by basketing through a steerable catheter and balloon dilatation
of stricture
tially successful Extracorporeal
have
been
[25, 26, 43]. shock-wave
tried,
biliary
and results
lithotripsy
were
par-
is a recog-
nized method for treating bile duct stones when other methods have failed; its success rate has been as high as 93% [44-46]. The technique may be useful as an adjunct to percutaneous radiologic technique. Nothing is perfect in the
management of bile duct stones in OCH, as was noted by vanSonnenberg et al. [25]: “While surgical and radiological techniques are jointly beneficial, the ultimate panacea for OCH may be medical control of biliary lithogenic factors.”
ACKNOWLEDGMENTS I thank material; Hee
University
tographs; script
my Yong
colleagues Koo
Park,
Hospital,
in our
department
Department for
preparation
collection Pathology,
of specimens
and Sung Sock Won for secretarial
preparation.
for
of Anatomic
and
assistance
of
case Kyung
microphoin manu-
8
LIM
AJR:157,
REFERENCES
Gastroentero!ogy
1977;72:
July 1991
630-633
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cholangitis.
Br J Surg 1954;42: 188-203 Ong GB. A study of recurrent pyogenic cholangitis. Arch Surg 1962;84: 199-225 Seel DJ, Park YK. Oriental infestational cholangitis. Am J Surg 1983;146: 188-203 carmona RH, Crass RA, Lim RC, Trunkey DD. Oriental cholangitis. Am J Surg 1984;148:117-124 Ho CS, Wesson DE. Recurrent pyogenic cholangitis in Chinese immigrants. AJR 1974;122:368-374 Menu Y, Lorphelin J-M, Scherrer A, Grenier P, Nahum H. Sonographk and computed tomographic evaluation of intrahepatic calculi. AiR 1985;145:579-583 Schulman A. Non-Western pattern of biliary stones and the role of ascariasis. Radiology 1987;162:425-430 Chou ST. Chan CW. Recurrent pyogenic cholangitis: a necropsy study. Pathology 1980;12:415-428 KaIser MH, Block MA. Cholangitis. In: Berk JE, ed. Bockus gastroenterology, 4th ed. Philadelphia: Saunders, 1985:3721-3723 Chau EMT, Leong LY, Chan FL. Recurrent pyogenic cholangitis: ultrasound evaluation compared with endoscopic retrogade cholangiopancreatography. Clin Radio! 1987;38:79-85 Lim JH, Ko YT, Lee DH, Hong KS. Oriental cholangiohepatitis: sonographic findings in 48 cases. AiR 1990;155:511-514 Chan F-L, Man S-W, Leong LLY, Fan S-T. Evaluation ofrecurrent pyogenic cholangitis with CT: analysis of 50 patients. Radiology 1989;170: 165-1 69 KaIser MH, Schoenfleld U, Marks JW, Tompkins RK. Cholelithiasis. In: Berk JE, ed. Bockus gastroenterology, 4th ed. Philadelphia: Saunders, 1985:3619-3624 Koge A, lchimiya H, Yamaguchi K, Miyazaki K, Nakayama F. Hepatolithiasis associated with cholangiocarcinoma. Possible etiologic significance. Cancer 1985;55:2826-2829 Chen M-F, Jan V-V. Wang C-S, Jeng L-B B, Hwang T-L, Chen S-C. Intrahepatic stones associated with cholangiocarcinoma. Am J Gastroentero! 1989;84:391-395 Nakanuma Y, Terada T, Tanaka Y, Ohta G. Are hepatolithiasis and cholangiocarcinoma aetiologically related? Virchows Arch [A] 1985;406: 48-58 Ho PC. The pathology of C!onorchis sinensis infestation of the liver. J
Patho! 1955;70:53-64 Lim JH, Ko VT, Lee DH, Kim SY. Clonorchiasis: sonographic findings in 59 proved cases. AJR 1989;152:761-764 19. Teoh TB. A study of gallstones and included worms in recurrent pyogenic cholangitis. J Pathol 1963;86:123-129 20. Rim HJ. The current pathobiology and chemotherapy of clonorchiasis. Korean J Parasito! 1986;24[suppl]:7-20 21. Flavell DJ. Liver-fluke infection as an aetiological factor in bile duct carcinoma of man. Trans R Soc Trop Med Hyg 1981;75:814-824 22. Matsushiro T, Suzuki N, Sato T, Mark T. Effect of diet on glucaric acid concentration in bile and the formation of calcium bilirubinate gallstones. 18.
24. 25.
26. 27. 28.
stones: a clinical study. Ann Surg 1972;175: 166-1 76 Chang TM, Passaro E. Intrahepatic stones: the Taiwan experience. Am J Surg 1983;146:241-244 vanSonnenberg E, Casola G, Cubberiey DA, et al. Oriental cholangiohepatitis: diagnostic imaging and interventional management. AiR 1986;146:327-331 Park JH, Chol BI, Han MC, Sung KB, Choo 1W, Kim C-W. Percutaneous removal of residual intrahepatic stones. Radiology 1987;163:619-623 RaIls PW, COIletti PM, Quinn MF, Lapin SA, Morris UL, Halls J. Sonography in recurrent oriental pyogenic cholangitis. AiR 1981;136: 101 0-1 012
Lee JT, Yoo HS, Kim KW, Lee DV, Lee YH, Suh JH. The capability of realtime ultrasound in the detection of the biliary tract stones. J Korean Soc Med Ultrasound 1986;5:33-40 29. Federle MP, Cello JP, Laing FC, Jeffrey RB. Recurrent pyogenic cholangitis in Asian immigrants. Radiology 1982;143: 151-1 56 30. tel Y, Araki T, Furui 5, Tasaka A, Atomi Y, Kuroda A. Computed tomography and ultrasound in the diagnosis of intrahepatic calculi. Radiology 1980;136:399-405 31 . Wastie ML, Cunningham IGE. Roentgenologic findings in recurrent pyogenic cholangitis. AJR 1973;1 19:71-77 32. Lam SK, Wong KP, Chan PKW, Ngan H, Ong GB. Recurrent pyogenic cholangitis: a study by endoscopic retrograde cholangiography. Gastroentero!ogy 1978;74: 1196-1203 33. Lim JH, Voon YK, Kim SY, Mm VI. Endoscopic retrograde cholangiographic findings in choledocholithiasis. J Korean Radio! Soc 1982;1 8:116-124 34. Letoumeau JH, Thompson WM. lntraoperative and postoperative cholangiography. Semin Ultrasound 1987;8: 126-1 33 35. Hong KS, tim JH, Ko VT, Lee DH. Endoscopic retrograde cholangiography in recurrent pyogenic cholangitis. J Korean Radio! Soc 1990;26: 1 17-1 20 36. Choi BI, Kim HJ, Han MC, Do YS, Han MH, Lee SH. CT findings of clonorchiasis. AiR 1989;152:281 -284 37. Chol TK, Wong KP, WongJ. Cholangiographicappearance in clonorchiasis. Br J Radio! 1984;57:681 -684 38. Lim JH. Radiologic findings of clonorchiasis. AJR 1990;155: 1001-1008 39. Ferrucci JT, Adson MA, Mueller PR, Stanley RJ, Stewart ET. Advances in the radiology ofjaundice: a symposium and review. AJR 1983;141 :1-20 40. Mittelstaedt CA, Volverg FM, Fischer GJ, McCartney WH. Caroli’s disease: sonographic findings. MR 1980;134:585-587 41 . Mujahed Z, Glenn F, Evans JA. Communicating cavernous ectasia of intrahepatic ducts (Caroli’s disease). AJR 1971;113:21-26 42. Vaira 0, D’Anna L, Ainley C, et al. Endoscopic sphincterotomy in 1000 consecutive patients. Lancet 1989;2:431-433 43. Kerlan AK Jr, Progany C, Goldberg HI, Ring EJ. Radiologic intervention in Oriental cholangiohepatitis. AiR 1985;145:809-813 44. Lee SH, Fache JS, Burhenne HJ. The value of extracorporeal shock-wave lithotripsy in the management of bile duct stones. AiR 1990;155:775-779 45. Moody FG, Amerson JR, Berci G, et al. Lithotripsy for bile duct stones. Am J Surg 1989;158:241-247 46. Choi BI, Han JK, Park VH, Voon YB, Han MC, Kim C-W. Piezoelectric lithotripsy combined with stone extraction in the management of retained intrahepatic stones. Radiology 1991;1 78:105-108
1
Review
.
Article
.
Oriental Cholangiohepatitis: Radiologic Features
Pathologic,
Clinical,
and
Jae Hoon Lim1
Oriental cholangiohepatitis, an endemic disease in Southeast Asia, is characterized by recurrent attacks of abdominal pain, fever, and jaundice. Pathologically, the intra- and extrahepatic ducts are dilated and contain soft, pigmented stone and pus. There is proliferation of bile ducts and infiltration of inflammatory cells along the periportal spaces and hepatic parenchyma. Localized intrahepatic segmental ductal stenosis may be present, especially in the lateral segment of the left lobe or posterior segment of the right hepatic lobe. The cause of the disease is not known, but associations with clonorchiasis, ascariasis, and nutritional deficiency have been suggested. Sonographic and CT findings include intra- or extrahepatic duct stones, dilatation of the extrahepatic duct with relatively mild or no dilatation of the intrahepatic ducts, localized dilatation of the lobar or segmental bile ducts, increased periportal echogenicity, segmental hepatic atrophy, and gallstones. Cholangiographic findings include bile duct stones; disproportionately severe dilatation of the extrahepatic ducts with mild or no dilatation of the intrahepatic ducts; and focal strictures, acute peripheral tapering, straightening, ngidity, decreased arborization, and an increased branching angle of the intrahepatic bile ducts.
Oriental cholangiohepatitis (OCH), also known as oriental cholangitis, recurrent pyogenic cholangitis, and intrahepatic pigmented stone disease, is characterized by recurrent attacks of fever, chills, abdominal pain, and jaundice [1-4]. Bile ducts are dilated or focally stenotic, harboring soft, pigmented stone or mud, and enteric bacteria can be cultured from the bile [1-3, 5]. The wall of the bile ducts is thickened by fibrosis and inflammatory cell infiltration. The disease is endemic to Received
December
Department
26, 1990;
of Diagnostic
accepted
Radiology,
after Kyung
revision
February
Hee University
Southeast
Asian countries [1-5], but sporadic cases have in Europe [6] and South Africa [7]. The disease encountered more often in western societies, especially in the United States and Canada, largely as a result of increased immigration from Asian countries [4, 5]. The purpose of this article is to review the sonographic, CT, and cholangiographic findings of OCH in light of the pathophysibeen reported is now being
Fig. 1.-Microphotograph of resected liver specimen shows soft, pigmented stone (long arrow) in dilated medium-sized bile duct. Note also severe thickening of small bile ducts and periductal fibrosis (short arrows) obliterating lumen of bile ducts and encroaching on hepatic parenchyma. (Masson’s trichrome stain, original magnification x8)
14, 1991.
Hospital,
1, Hoeki-dong,
LJm. AJR 157:1-8,
July
1991 0361-803X/91/1571-0001
© American
Roentgen
Ray Society
Dongdaemun-ku,
Seoul
130-702,
Korea.
Address
reprint
requests
to J. H.
LIM
2
ology of the disease and to discuss the management of the disease.
the radiologist’s
role in
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Pathology
The primary pathologic changes are in the bile ducts. Histologically [1 2, 8], there is proliferation of bile ducts, and inflammatory cells, mostly polymorphonuclear leukocytes, infiltrate from the portal tracts well into the hepatic parenchyma, accompanied by local hepatocellular necrosis. In more severe cases this inflammation undergoes suppuration. Fibrous tissue proliferates in the portal tracts, especially around the bile ducts (Figs. I and 2). The intrahepatic ducts frequently show dilatation and stricture and may contain pigmented stone (Fig. 1), pigmented mud, and debris and may shed epithelial cells, exudates, and sometimes frank pus. Liver changes are common and can be quite severe [2, 9]. The liver is usually enlarged and scarred, and capsular adhesions are evident. Occasionally, after multiple attacks, the liver becomes shrunken, especially the lateral segment of the left lobe. The papilla is usually hypertrophied [2], fibrosed, and rigid but ,
patent,
allowing
passage
of a large
dilator
without
difficulty
[9]. In some cases there is penampullary stricture due to fibrosis and passage of stone. Dilatation of the extrahepatic ducts and large intrahepatic ducts such as the right and left hepatic ducts is observed in most patients (85-1 00%) [1 0, 1 1]. Dilatation of the intrahepatic biliary ducts tends to be disproportional, that is, central dilatation with rapid tapering toward the periphery [1 0]. The first and second divisions of the ducts are dilated, whereas the third and fourth divisions are not. The cause is not known, but periductal diffuse fibrosis may play a role (Fig. 2). This pattern
of bile duct
dilatation
is quite
different
from
the dila-
tation caused by obstruction. In obstruction, the intrahepatic bile ducts are dilated diffusely instead of rapidly tapering peripherally. The dilatation of the extrahepatic duct generally is not related to the location of the stone [1 1]. Ducts both proximal and distal to the stone are dilated diffusely. Repeated passage of small pieces of stones through the sphincter of Oddi into the duodenum results in hypertrophy, ulceration, and stricture [2],
and these
changes
may
cause
stenosis
and
MR:157,
July 1991
hepatic ducts or both. Occasionally the bile ducts are packed with stones. Bile duct stones are present in about 75-80% of cases [2, 9]. In the remaining cases, the biliary tree is infected recurrently in the absence of stone. Gallstones are found frequently, and including the cases of previous cholecystectomy, gallstones are present in about 50-70% [10-12]. The reported prevalence of cholangiocarcinoma associated with
OCH
ranges
from
2.4%
to
5.0%
[1 4,
15].
Chronic
proliferative cholangitis in the presence of bile duct can undergo progressive changes to atypical epithelial plasia,
which
may
progress
to cholangiocarcinoma
stones hyper[1 6]. To
my knowledge there has been no report on an increased prevalence of hepatocellular carcinoma in patients with OCH.
Pathogenesis
Two theories esis of OCH.
have been advanced Chronic
infestation
to explain the pathogen-
of the biliary
tree
with
en-
demic parasites such as Clonorchis sinensis and Ascaris lumbricoides may induce ductal injury and strictures, leading to stone formation. Many patients with intrahepatic stone have evidence
tation
of clonorchiasis
with Ascaris
Microscopic
sections
[1
is observed of stones
,
1 7, 1 8]. Evidence
in patients from
extra-
with
of infes-
OCH
[7].
and intrahepatic
bile ducts revealed evidence of C. sinensis (Fig. 3) and A. lumbricoides [1 1 9]. As adult flukes or Ascaris eggs and ,
desquamated
epithelial
cells block
the intrahepatic
ducts
par-
tially or completely, tion favors bacterial
bile stasis is sure to follow [17]. Stagnainfection resulting in pyogenic cholangitis. pyogenic infection occurs in the bile ducts, C. sinensis are killed [17, 20]. Bile stasis and the presence of dead and ova or their debris can form a nucleus (Fig. 3) for
When flukes flukes the formation of gallstones or bile duct stones [19], and this could instigate all the consequent pathologic processes, resuiting in a cycle of repeated bouts of cholangitis and stone formation [3]. The formation of bilirubin stones may be attributed to bacterial deconjugation of bilirubin diglucuronoside
proximal
dilatation. However, localized stricture and resultant dilatation of the intrahepatic ducts are closely related to the location of stones. The left lateral segmental duct is affected earlier and more severely [2, 1 1 1 2], followed by the posterior segmental duct of the right lobe [12]. This may be related to the more acute angulation of these ducts, resulting in less efficient drainage on this side of the biliary system [2, 12]. Stricture along the extrahepatic ducts is very unusual [2]. The bile duct stones encountered in western persons originate in the gallbladder and have the same chemical composition as gallstones [13]. On the other hand, the stones in ,
patients with OCH originate in the bile ducts and are composed mostly of bile pigment with variable calcification. The stones are dark brown or black and vary in consistency from claylike, muddy material to concrete stones that are usually soft and friable [2, 3, 9]. There may be single or multiple stones. Multiple stones are scattered in the intra- or extra-
Fig. 2.-Cut surface of resected lateral segment of left hepatic lobe shows marked fibrous thickening of segmental bile duct (open arrows) and its tributaries. Hepatic veins (solId arrows).
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MR:157,
ORIENTAL
July 1991
CHOLANGIOHEPATITIS
with the formation of insoluble bilirubin during bouts of cholangitis [21]. Ong [2], however, found that patients with OCH had only a 5% higher rate of infestation with C. sinensis than did patients in general outpatient clinics. Large proportions of persons in endemic areas are infested with liver flukes without pyogenic cholangitis developing [8]. It was proposed that the primary cause was portal septicemia resulting from poor eating habits [2, 4]. Ong [2] believed infection reached the biliary tract from the portal vein: “The infection having reached the liver is excreted into the bile. Should there be obstruction by C. sinensis, tumor or stones, cholangitis would be the result.” This theory was supported by animal experiments [8]. Bilirubinate stones may be formed in the liver as a result of an increase in deconjugation of bilirubin glucuronide by Escherichia co/i, attributed to a net increase in f.-glucuronidase activity. This arises when the intrahepatic environment is deficient in glucaric acid, a fl-glucuronidase inhibitor that is lacking in a low-protein diet [22]. These two theories cannot explain the pathogenesis of OCH. Perhaps both factors play a role separately or synergistically.
Clinical
Manifestations
Men and women are affected almost equally [2, 9] and the highest number of cases occur in persons 20-40 years of age. There is a strong association with lower socioeconomic class. The symptoms are recurrent attacks and remissions of abdominal pain, nausea, vomiting often accompanied by fever, shaking chills, and jaundice. Visible jaundice is present in 77% of patients [2]. Physical examination reveals epigastric tenderness and rigidity and enlargement of the liver and gallbladder. Occasionally patients with severe disease such as sepsis present with shock and mental confusion. Laboratory findings are leukocytosis, predominantly polymorphonuclear leukocytes; elevated levels of alkaline phosphatase; and excretion of urobilinogen in urine. Bile cultures yield E. co/i or other enteric bacteria. The natural history of the disease is marked by recurrent attacks of cholangitis, usually once or twice a year [2, 9]. Many of the acute attacks respond to antibiotic treatment; many also require decompression of the biliary tree after control of the acute attack [2, 9], especially when there is a stone or stricture of bile ducts. OCH is a frequent reason for emergent surgery in the endemic areas. Recurrent disease is common postoperatively, especially when the operation does not include a drainage procedure [4, 23-25]. Even after surgery with drainage, stones and stricture return and the attacks of cholangitis recur sooner or later. In a study of 115 patients who had had surgery, 66 patients (57%) had residual intrahepatic stones [26]; biliary stricture caused the remnant stone in the majority of cases (81%).
Radiologic
Fig. 3.-Microphotograph embedded In pigmented
stone.
shows eggs of Clonorchls slnensls (arrows) (H and E, original magnification xlOO)
Fig. 4.-Sagittal sonogram shows dilatation of common bile duct containing three shadowing stones (arrows). Wall of common bile duct (D) is thick.
Fig. 5.-Transverse sonogram of liver shows a shadowing echogenic cast filling posterior segmental bile duct of right hepatic lobe (arrows).
3
Findings
Radiologic assessment of the biliary tree is imperative if the correct preoperative evaluation is to be made regarding the need for and the type of surgery [4, 25]. Plain radiography is not helpful because the stones are rarely radiopaque [2, 6, 7, 12]. Oral cholecystography, IV cholangiography, and biliary scintigraphy are not useful [2,27]: correct anatomic diagnosis cannot be made even if the biliary tract is visualized.
4
LIM
MR:157,
July 1991
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Fig. 6.-Transverse sonogram of common bile duct shows a round, nonshadowing stone (arrow). Proximal and distal portions of bile duct are dilated diffusely (arrowheads). A = abdominal aorta, v = inferior vena cava.
Fig. 7.-Transverse sonogram of left hepatic lobe shows thickening and increased echogenicity of walls of bile ducts (arrows) and umbilical portion of left portal vein (P).
Sonographic
Findings
Sonography delineates bile duct dilatation in virtually all patients with OCH. The extrahepatic bile ducts are dilated in 85-100% of cases and the larger intrahepatic bile ducts are dilated in 66-79% of cases [1 0, 1 1 ]. Usually, the smaller intrahepatic bile ducts such as the tertiary or quaternary divisions proximal to the segmental bile ducts are dilated only slightly or not at all. In general, the dilatation of the extrahepatic duct is not related to the location of stone [1 1], although localized dilatation of the intrahepatic ducts is closely related to the location of stricture and stone Iodgment, especially the lateral segmental ducts of the left hepatic lobe [1 1]. In a large proportion of patients with OCH (85-90%), a stone or stones can be detected with sonography [1 0, 1 1]. The stones may be in either the extrahepatic (Fig. 4) or intrahepatic (Fig. 5) ducts or both. In some cases, stones are only in the segmental bile ducts, such as the lateral segment of the left hepatic lobe or posterior segment of the right hepatic lobe (Fig. 5). The stones may be more echogenic than the liver parenchyma Some
and
adjacent
usually
echogenic
tissue
or,
less
commonly,
isoechoic.
stones cast shadow and some do not, even in the same patient [1 0, 1 1]. In general, the intrahepatic stones are extrahepatic
and
shadowing
(Fig.
5), whereas
some
stones
(25%) do not cast shadow (Fig. 6). This may be due to the poor rate of detection of the intrahepatic stones, because hypoechoic intrahepatic stones without shadows can be missed on sonography. The detectability of stones with sonography depends on the size, echogenicity, shadowing characteristics, and location of the stones [11, 28]. Biliary mud or isoechoic bile duct stones filling the biliary tree as a cast can be missed because sometimes they appear as soft-tissue masses and obscure visualization of intrahepatic ductal dilatation [10, 25, 29]. Biliary pneumatosis, as a result of prior choledochoenteric anastomoses or sphincter incompetency, obscures visuali-
zation of stone. A higher proportion of nonshadowing stones in the extrahepatic ducts can be detected compared with intrahepatic stones [10, 11]; this is because the duct is dilated, providing a larger space to enable the nonshadowing stone to be detected (Fig. 6).
Fig. around
8.-CT ports
scan hepatis,
shows dilatation of central intrahepatic with bile ducts tapering abruptly toward
bile ducts periphery.
Chau et al. [1 0] described prominent periportal echogenicity (Fig. 7) representing pericholangitis and periportal fibrous thickening in 30% of their cases. Gallstones are found frequently patients
[1 0, 1 1]. Hepatic abscess or biloma complications with OCH can be delineated on sonograms.
in
CT Findings The optimal CT technique
is enhanced
scanning
with a slice
thickness scanning
of 5 mm and 2-mm interslice gap. Unenhanced may be helpful in detecting stones. CT demonstrates the full extent of ductal dilatation [12]. Dilatation of the extra-
hepatic ducts is depicted clearly. Central, larger intrahepatic biliary dilatation; acute peripheral tapering; and nonvisualization toward the periphery of the liver give rise to the characteristic arrowhead appearance on contiguous sections (Fig. 8). There may be localized dilatation from obstruction by stricture (Fig. 9) or stone, such as that of lateral segmental ducts of the left hepatic lobe and posterior segmental ducts of the right hepatic lobe [12]. However, biliary strictures,
which are usually
short
segments,
are difficult
to depict
be-
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MR:157,
July 1991
ORIENTAL
5
CHOLANGIOHEPATITIS
Fig. 9.-Multiple intrahepatic stones in lateral segment of left lobe and extrahepatic stone. A, Transverse sonogram of epigastrium shows shadowing echogenic foci (short arrow). Note moderate dilatation of subsegmental bile duct with thick wall (long arrow). B, CT scan of liver shows localized severe dilatation of lateral segmental bile duct of left hepatic lobe due to localized stricture (arrow). Multiple tiny high-density areas within dilated duct represent small stones that might have been overlooked on basis of CT alone. Wall of dilated bile ducts is enhanced. C, CT scan at level of pancreatic head shows small, round, calcified stone (arrow) within dilated intrapancreatic common bile duct.
Fig. 10.-CT scan shows cystically dilated bile duct containing stone. Wall of dilated bile duct is enhanced. Biliary pneumatosis (arrow). The patient had had a cholecystectomy.
Fig. 11.-Enhanced CT scan shows homogeneous enhancement of left lobe of liver. Walls of bile ducts are enhanced (long arrows). lntrahepatic stones (short arrows) have same attenuation as liver. PV = right branch of portal vein.
Fig. 12.-CT scan shows severe atrophy of lateral segment of left hepatic lobe harboring small calcific stones (open arrow).
cause of partial-volume averaging. Sometimes, dilatation may be fusiform or cystic (Fig. 10). The wall of the bile ducts may enhance on CT scans obtained with contrast material (Figs. 9 and 10), especially during an acute cholangitic episode [12]. The stones can be depicted with CT, but the detection rate (63-81%) is generally not as good as that of sonography [6, 30]. It has been stated that unlike cholesterol stones, which may be isodense with bile, pigmented stones are hyperdense on CT (Fig. 9C) because of their variable content of calcium salts, heavy metals, and other inorganic components [29, 30].
completely fill the ducts within the hepatic parenchyma (Fig. 11) could easily be missed on CT; in these patients, even the dilated bile ducts are difficult to recognize. Chan et al. [12]
However, bile duct stones are sometimes not sufficiently hyperdense to be visualized on CT (Fig. 11). Often the stones are hypodense, and thus it is impossible to distinguish stones
exacerbation,
from bile or pus in the dilated duct [30]. Isodense
stones that
described both unenhanced and enhanced scans as desirable because stones are detected more easily on unenhanced scans, and enhanced CT scans are better in the detection of
subtle intrahepatic biliary dilatation. In addition to the ductal change and detection of stones, parenchymal loss and segmental atrophy (Fig. 12) can be correctly assessed with CT [12]. During the stage of acute persistent
segmental
or lobar
parenchymal
en-
hancement can be observed (Fig. 11), suggesting diffuse parenchymal inflammation or microabscess [12]. Frank hepatic abscess or biloma can be delineated.
LIM
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6
AJR:157,
July 1991
Fig. 13.-Endoscopic retrograde cholanglogram shows three stones with facets. Extrahepatic ducts are markedly dilated. Right and left hepatic ducts and their first divisions are moderately dilated but more peripheral ducts taper abruptly. Intrahepatic bile ducts show straightening and rigidity, right angle branching pattern, decrease in arborization, and acute peripheral tapering. (Reprinted from Lim et al. [11].)
Fig. 14.-Endoscopic retrograde cholanglogram shows mild dilatation of extra- and intrahepatic bile ducts with abrupt peripheral tapering, straightening, and increased angle of branching. Three small faceted stones are seen in common bile duct (whIte arrows). Lateral segmental bile duct of left hepatic lobe is diffusely dilated and harbors multiple filling defects of stones (arrowheads). Note mild stricture at juncton (black arrow) of lateral segmental duct and left lobar ducts.
ducts (Figs. 13 and 1 4). When the stones completely obstruct the orifice of the segmental or subsegmental bile ducts (missing duct sign), the stone cannot be detected (Fig. 15). Similarly, when there is a stricture at the segmental or subsegmental bile ducts, proximal bile ducts cannot be opacified, leading to an erroneous interpretation of no ductal stone or stricture [27]. A few patients (15-25%) have no stones, or stones pass spontaneously [2]; in these patients, the characteristic pattern of the biliary tree will lead to the correct diagnosis [35].
diagnosis between gallstones passed into the extrahepatic duct and OCH is very difficult. The stone passed only into the extrahepatic duct from the gallbladder usually will result in dilatation mainly proximal to the stone [34], whereas in OCH the extrahepatic ducts both proximal and distal to the stone are dilated diffusely regardless of the level of the stone [33, 35]. Clonorchiasis, another prevalent infestational disease in the same endemic areas, causes diffuse dilatation of the intrahepatic bile ducts with no or minimal dilatation of the large bile ducts; these changes are easily recognizable on sonography [1 8], CT [36], and cholangiography [37, 38]. Periductal changes are encountered in both diseases, but are much more severe in clonorchiasis. Stones and flukes of C. sinensis can be differentiated easily. In biliary obstruction by malignant tumors along the bile ducts, including cholangiocarcinoma and cancer of the pancreas or ampulla of Vater, the entire biliary tree proximal to the mass is dilated, including peripheral intrahepatic bile ducts, and an obstructing mass can be detected [1 1 8, 38]. Sclerosing cholangitis may show bile duct dilatation and thickening of all of the bile ducts, but dilatation is focal and discontinuous, sometimes having a beaded appearance and serpiginous course [39]. Caroli disease is a developmental anomaly in which there is segmental saccular dilatation of the intrahepatic ducts. This results in stasis, cholangitis, liver abscess, and stone formation. The clinical picture is similar to that of OCH, but it occurs in a younger age group. Differentiation is possible by noting the dilated saccules in the intrahepatic bile ducts [40, 41].
Differential
Relative Roles of Imaging
Cholangiographic
Findings
Direct cholangiography, such as endoscopic retrograde cholangiography, percutaneous transhepatic cholangiography, operative cholangiography, and T-tube cholangiography, demonstrates the full spectrum of ductal changes and stones in patients with OCH (Fig. 13). Abnormal findings include disproportionately severe dilatation of the extrahepatic ducts with mild or no dilatation of the intrahepatic ducts and acute tapering, straightening, rigidity, increased or right-angle branching pattern, multiple focal strictures, and decrease in arborization [31 -35]. These abnormalities are due to fibrosis and scarring of bile ducts [5]. Biliary duct dilatation is segmental or subsegmental [31 ] when there is stricture of intrahepatic bile ducts or obstruction by impacted stone (Fig. 14). Stricture of the extrahepatic bile ducts may occur, but this is unusual. Rarely, the segmental or subsegmental bile ducts dilate cystically because of persistent obstruction, resultant inflammation, and loss of the elasticity of the ducts. Stones
produce
negative
filling defects
in the opacified
bile
,
Diagnosis
From the radiologic point of view, OCH is characterized by the presence of stone(s), dilatation of the extrahepatic ducts, large intrahepatic bile ducts with acute peripheral tapering, and thickening of the wall of bile ducts. Knowing these features, radiologic differentiation from other diseases of the bile ducts can be possible. In western patients, the differential
Tests
Sonographic evaluation of extrahepatic bile duct dilatation is easy, although duodenal gas sometimes hinders the visualization of the whole segment, especially the distal common bile duct. Most intra- and extrahepatic stones are recognized easily. However, those stones that do not cast an acoustic shadow are difficult to recognize unless corresponding ducts
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AJR:157,
ORIENTAL
July 1991
7
CHOLANGIOHEPATITIS
Fig. 15.-Remnant stone after surgical removal of some stones. A, Sonogram of right hepatic lobe discloses a bandlike shadowing stone (arrows) filling posterior segmental bile duct. B, During surgery, several small pigmented stones were removed. Operative cholangiogram does not show any stone in biliary review suggests an area is devoid of bile ducts (missing duct sign, arrow) in lateral part of right hepatic lobe. C, T-tube cholangiogram discloses large stones packing markedly dilated posterior segmental duct of right hepatic lobe (arrows). posterior segmental duct joining right hepatic duct.
Retrospective
Note
hairpin
turn of
are markedly dilated [1 0, 1 1 ]. Bile duct stricture cannot be demonstrated easily. In the presence of biliary pneumatosis, bile ducts and stones are difficult to assess [25, 29]. CT demonstrates the full extent of ductal abnormality [12]. Biliary dilatation and isolated segmental or subsegmental
Role of Interventional
biliary
usually is essential [23-25]. In emergent cases with increased risk of surgical mortality, biliary decompression with a percu-
dilatation
can
be recognized
easily.
However,
it is
relatively insensitive in depicting stones. Pneumatosis, parenchymal enhancement, and segmental atrophy can be assessed by CT. However, biliary strictures, which usually are less than 1 cm long or are diaphragmlike, and ductal wall irregularities often are not diagnosed with CT [12]. Cholangiography
the biliary sometimes especially
is straightforward,
as it directly
delineates
tree, including stones and strictures. However, it is difficult to visualize the whole biliary tree, when
there
is technical
failure
in the opacification
of the whole biliary tree or obstruction due to ductal stricture or impaction of stones, leading to an erroneous normal interpretation. Sonography should be the main technique used for screening and diagnosis in suspected OCH [10-12, 27, 29]. CT is not a screening procedure, but it is recommended when sectional imaging is mandatory but sonography is not confirmative or is equivocal, when space-occupying lesions complicate OCH, when hepatic resection is planned, and when imaging guidance is needed for complex drainage procedures or formation of safe access to an anastomotic loop of a bowel [12]. Direct cholangiography, although invasive, is mandatory as a “road map” in patients undergoing surgical intervention, because the exact location and number of stones and bile duct strictures must be assessed preoperatively [6]. Cholangiography is necessary for the detection of residual stones after surgery, assessment of biliary stricture and choledochoenteric fistulas, and preprocedural biliary intervention [25, 26].
Radiology
tree.
in the Management
of
Bile Duct Stones Surgery controlled
taneous
used to remove stones after [2, 9]. At surgery, an internal
catheter
is the procedure
acute cholangitis is drainage procedure
of choice.
There are several nonsurgical means of treating bile duct stones and stricture. Flexible choledochoscopy and endoscopic papillotomy [42] have been used to remove postoperative residual stones. Recently, percutaneous removal of stones by basketing through a steerable catheter and balloon dilatation
of stricture
tially successful Extracorporeal
have
been
[25, 26, 43]. shock-wave
tried,
biliary
and results
lithotripsy
were
par-
is a recog-
nized method for treating bile duct stones when other methods have failed; its success rate has been as high as 93% [44-46]. The technique may be useful as an adjunct to percutaneous radiologic technique. Nothing is perfect in the
management of bile duct stones in OCH, as was noted by vanSonnenberg et al. [25]: “While surgical and radiological techniques are jointly beneficial, the ultimate panacea for OCH may be medical control of biliary lithogenic factors.”
ACKNOWLEDGMENTS I thank material; Hee
University
tographs; script
my Yong
colleagues Koo
Park,
Hospital,
in our
department
Department for
preparation
collection Pathology,
of specimens
and Sung Sock Won for secretarial
preparation.
for
of Anatomic
and
assistance
of
case Kyung
microphoin manu-
8
LIM
AJR:157,
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